{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T20:46:18Z","timestamp":1789245978682,"version":"build-2803163510"},"reference-count":44,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T00:00:00Z","timestamp":1699315200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Klebsiella spp. can colonize the intestine of preterm neonates, and over-growth has been associated with necrotizing enterocolitis, hospital-acquired infections, and late-onset sepsis. This could lead us to suggest that the clinical pertinence of intestinal colonization with <jats:italic>ESBL<\/jats:italic> in preterm neonates appears to be important. We conducted this study to characterize the genetic proprieties <jats:italic>of ESBL-producing<\/jats:italic> <jats:ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"https:\/\/www.sciencedirect.com\/topics\/medicine-and-dentistry\/klebsiella\" xlink:type=\"simple\"><jats:italic>Klebsiella<\/jats:italic><\/jats:ext-link> <jats:italic>pneumoniae (ESBL-KP)<\/jats:italic> under clinical isolates and to describe the risk factors for the intestinal tract acquisition event during hospitalization.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>One hundred and thirteen premature infants were recruited from the neonatal intensive care unit (NICU). All newborns are issued from the birth suites of the pregnancy department. Two rectal swabs were planned to define <jats:italic>K<\/jats:italic>. <jats:italic>Pneumoniae<\/jats:italic> intestinal carriage status. ESBL-KP was confirmed by Brilliance <jats:italic>ESBL<\/jats:italic> selective chromogenic Agar. Antimicrobial susceptibility testing including phenotypic testing and genotypic detection of the most commonly described ESBL genes was done. Logistic regression models were performed to find the variables associated with the acquisition event of <jats:italic>ESBL-KP<\/jats:italic>.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>A total of 62 (54.86%) premature neonates were colonized with <jats:italic>ESBL-KP<\/jats:italic>. The rate of <jats:italic>blaSHV<\/jats:italic>, <jats:italic>blaTEM<\/jats:italic>, <jats:italic>blaCTX-M1<\/jats:italic>, <jats:italic>blaCTX-M2<\/jats:italic>, <jats:italic>blaCTX-M9<\/jats:italic>, <jats:italic>and blaOXA-48<\/jats:italic> genes among the isolates was 82, 48, 93.5, 4.8, 11.2 and 3.22%, respectively. We found that <jats:italic>ESBLs K<\/jats:italic>. <jats:italic>Pneumoniae<\/jats:italic> isolates were 100% resistant to <jats:italic>amoxicillin<\/jats:italic>, <jats:italic>clavulanic acid-amoxicillin<\/jats:italic>, <jats:italic>cefotaxime<\/jats:italic>, <jats:italic>ceftazidime<\/jats:italic>, and <jats:italic>gentamicin<\/jats:italic>. The regression model is for a given significant association between the tract intestinal of <jats:italic>ESBL-KP<\/jats:italic> acquisition events and the use of enteral tube feeding (OR = 38.46, 95% CI: 7.86\u2013188.20, p-Value: 0.001), and endotracheal tubes (OR = 4.86, 95% CI: 1.37\u201317.19, p-Value 0.014).<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusion<\/jats:title>\n<jats:p>Our finding supposes that the enteral feeding tube and endotracheal tube might have a critical role in colonizing the intestinal tract of preterm infants. This highlights the current status of both practices that will require updated procedures in the NICU.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0293949","type":"journal-article","created":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T18:23:31Z","timestamp":1699381411000},"page":"e0293949","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["Gut acquisition of Extended-spectrum \u03b2-lactamases-producing Klebsiella pneumoniae in preterm neonates: Critical role of enteral feeding, and endotracheal tubes in the neonatal intensive care unit (NICU)"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7070-8261","authenticated-orcid":true,"given":"Benboubker","family":"Moussa","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bouchra","family":"Oumokhtar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Btissam","family":"Arhoune","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdelhamid","family":"Massik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samira","family":"Elfakir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"Khalis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3432-5204","authenticated-orcid":true,"given":"Hammad","family":"Soudi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fouzia","family":"Hmami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,11,7]]},"reference":[{"issue":"13","key":"pone.0293949.ref001","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1056\/NEJMoa1306801","article-title":"Multistate Point-Prevalence Survey of Health Care\u2013Associated Infections","volume":"370","author":"SS Magill","year":"2014","journal-title":"N Engl J Med"},{"key":"pone.0293949.ref002","unstructured":"SURVEILLANCE REPORT. Surveillance of antimicrobial resistance in Europe 2018.: 110."},{"issue":"1","key":"pone.0293949.ref003","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1186\/1471-2334-13-466","article-title":"Predominance of Klebsiella pneumoniaeST14 carrying CTX-M-15 causing neonatal sepsis in Tanzania","volume":"13","author":"SE Mshana","year":"2013","journal-title":"BMC Infect Dis"},{"issue":"2","key":"pone.0293949.ref004","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.bjid.2019.03.002","article-title":"High prevalence of CTX-M-1 group in ESBL-producing enterobacteriaceae infection in intensive care units in southern Chile","volume":"23","author":"M Pavez","year":"2019","journal-title":"Braz J Infect Dis"},{"issue":"4","key":"pone.0293949.ref005","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1089\/mdr.2004.10.354","article-title":"Outbreak of SHV-5 \u03b2-Lactamase-Producing Klebsiella pneumoniae in a Neonatal-Pediatric Intensive Care Unit in Spain","volume":"10","author":"L Bri\u00f1as","year":"2004","journal-title":"Microb Drug Resist"},{"key":"pone.0293949.ref006","article-title":"Caracterizaci\u00f3n de cepas de Klebsiella pneumoniae productora de b-lactamasa de espectro extendido aisladas en dos unidades de cuidados intensivos","volume":"7","author":"AC Gonz\u00e1lez","journal-title":"Rev Chil Infectol"},{"issue":"12","key":"pone.0293949.ref007","doi-asserted-by":"crossref","first-page":"2613","DOI":"10.3390\/microorganisms9122613","article-title":"Colonization with Multidrug-Resistant Bacteria in the First Week of Life among Hospitalized Preterm Neonates in Serbia: Risk Factors and Outcomes","volume":"9","author":"M Milic","year":"2021","journal-title":"Microorganisms"},{"issue":"5","key":"pone.0293949.ref008","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1097\/ANC.0000000000000220","article-title":"Potential NICU Environmental Influences on the Neonate\u02bcs Microbiome: A Systematic Review","volume":"15","author":"LE Hartz","year":"2015","journal-title":"Adv Neonatal Care"},{"issue":"1","key":"pone.0293949.ref009","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s40168-015-0126-1","article-title":"The first microbial environment of infants born by C-section: the operating room microbes","volume":"3","author":"H Shin","year":"2015","journal-title":"Microbiome"},{"issue":"26","key":"pone.0293949.ref010","doi-asserted-by":"crossref","first-page":"11971","DOI":"10.1073\/pnas.1002601107","article-title":"Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns","volume":"107","author":"MG Dominguez-Bello","year":"2010","journal-title":"Proc Natl Acad Sci"},{"issue":"5","key":"pone.0293949.ref011","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1016\/j.chom.2015.04.004","article-title":"Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life","volume":"17","author":"F B\u00e4ckhed","year":"2015","journal-title":"Cell Host Microbe"},{"issue":"1","key":"pone.0293949.ref012","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1186\/1471-2334-9-146","article-title":"Neonatal enteral feeding tubes as loci for colonisation by members of the Enterobacteriaceae","volume":"9","author":"E Hurrell","year":"2009","journal-title":"BMC Infect Dis"},{"issue":"1","key":"pone.0293949.ref013","doi-asserted-by":"crossref","first-page":"54","DOI":"10.3109\/00365548.2012.713116","article-title":"Risk factors for acquisition of CTX-M-15 extended-spectrum beta-lactamase-producing Klebsiella pneumoniae during an outbreak in a neonatal intensive care unit in Norway","volume":"45","author":"S Rettedal","year":"2013","journal-title":"Scand J Infect Dis"},{"issue":"2","key":"pone.0293949.ref014","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1093\/tropej\/fmp060","article-title":"Risk Factors for Extended-Spectrum -Lactamase Producing Escherichia Coli and Klebsiella Pneumoniae Acquisition in a Neonatal Intensive Care Unit","volume":"56","author":"S Shakil","year":"2010","journal-title":"J Trop Pediatr"},{"key":"pone.0293949.ref015","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1128\/JCM.42.10.4769-4775.2004","article-title":"Dramatic Increase in Prevalence of Fecal Carriage of Extended-Spectrum \u2424-Lactamase-Producing Enterobacteriaceae during Nonoutbreak Situations in Spain","volume":"42","author":"A Valverde","year":"2004","journal-title":"J CLIN MICROBIOL"},{"issue":"4","key":"pone.0293949.ref016","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.ajic.2006.04.210","article-title":"Surveillance of multidrug-resistant gram-negative bacilli in a neonatal intensive care unit: prominent role of cross transmission","volume":"35","author":"C Mammina","year":"2007","journal-title":"Am J Infect Control"},{"key":"#cr-split#-pone.0293949.ref017.1","unstructured":"World Health Organization. Regional Office for South-East Asia. Preconception care. In: Regional expert group consultation 6-8 August 2013, New Delhi, India [Internet]. New Delhi: WHO Regional Office for South-East Asia"},{"key":"#cr-split#-pone.0293949.ref017.2","unstructured":"2014 [cited 2021 Oct 9]. https:\/\/apps.who.int\/iris\/handle\/10665\/205637."},{"key":"pone.0293949.ref018","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.jgar.2016.11.004","article-title":"Rectal carriage of extended-spectrum \u03b2-lactamase- and carbapenemase-producing Enterobacteriaceae among hospitalised neonates in a neonatal intensive care unit in Fez, Morocco","volume":"8","author":"B Arhoune","year":"2017","journal-title":"J Glob Antimicrob Resist"},{"issue":"9","key":"pone.0293949.ref019","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1099\/jmm.0.032482-0","article-title":"Characterization of extended-spectrum \u03b2-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates from the community in Morocco","volume":"60","author":"A Barguigua","year":"2011","journal-title":"J Med Microbiol"},{"issue":"1","key":"pone.0293949.ref020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.9734\/JAMB\/2018\/39955","article-title":"Antimicrobial Resistance Profile and Molecular Characterization of Extended-spectrum Beta-lactamase Genes in Enterobacteria Isolated from Human, Animal and Environment","volume":"10","author":"G Carole","year":"2018","journal-title":"J Adv Microbiol"},{"issue":"12","key":"pone.0293949.ref021","doi-asserted-by":"crossref","first-page":"3877","DOI":"10.1128\/JCM.02117-12","article-title":"Laboratory detection of Enterobacteriaceae that produce carbapenemases","volume":"50","author":"D Doyle","year":"2012","journal-title":"J Clin Microbiol"},{"key":"pone.0293949.ref022","doi-asserted-by":"crossref","DOI":"10.1128\/AAC.44.4.891-897.2000","article-title":"Characterization of VIM-2, a Carbapenem-Hydrolyzing Metallo- \u2424-Lactamase and Its Plasmid- and Integron-Borne Gene from a Pseudomonas aeruginosa Clinical Isolate in France","volume":"44","author":"L Poirel","year":"2000","journal-title":"ANTIMICROB AGENTS CHEMOTHER"},{"key":"pone.0293949.ref023","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fcimb.2018.00004","article-title":"Colonization, Infection, and the Accessory Genome of Klebsiella pneumoniae","volume":"8","author":"RM Martin","year":"2018","journal-title":"Front Cell Infect Microbiol"},{"issue":"3","key":"pone.0293949.ref024","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1128\/MMBR.00078-15","article-title":"Klebsiella pneumoniae: Going on the Offense with a Strong Defense","volume":"80","author":"MK Paczosa","year":"2016","journal-title":"Microbiol Mol Biol Rev"},{"issue":"3","key":"pone.0293949.ref025","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.jhin.2017.11.022","article-title":"Carriage of ESBL-producing Enterobacteriaceae in French hospitals: the PORTABLSE study","volume":"98","author":"B Pilmis","year":"2018","journal-title":"J Hosp Infect"},{"issue":"4","key":"pone.0293949.ref026","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.jhin.2018.03.017","article-title":"Routine screening for colonization by Gram-negative bacteria in neonates at intensive care units for the prediction of sepsis: systematic review and meta-analysis","volume":"99","author":"J Seidel","year":"2018","journal-title":"J Hosp Infect"},{"issue":"1","key":"pone.0293949.ref027","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.jpeds.2009.06.063","article-title":"Intestinal Microbial Ecology in Premature Infants Assessed with Non\u2013Culture-Based Techniques","volume":"156","author":"M Mshvildadze","year":"2010","journal-title":"J Pediatr"},{"issue":"12","key":"pone.0293949.ref028","doi-asserted-by":"crossref","first-page":"e27858","DOI":"10.1371\/journal.pone.0027858","article-title":"Beyond Bacteria: A Study of the Enteric Microbial Consortium in Extremely Low Birth Weight Infants","volume":"6","author":"MS LaTuga","year":"2011","journal-title":"PLoS ONE"},{"issue":"3","key":"pone.0293949.ref029","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1203\/01.PDR.0000134251.45878.D5","article-title":"Early Intestinal Bacterial Colonization and Necrotizing Enterocolitis in Premature Infants: The Putative Role of Clostridium","volume":"56","author":"MF de la Cocheti\u00e8re","year":"2004","journal-title":"Pediatr Res"},{"issue":"4","key":"pone.0293949.ref030","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/s40124-013-0031-7","article-title":"The Microbiome and its Impact on Disease in the Preterm Patient","volume":"1","author":"J. Neu","year":"2013","journal-title":"Curr Pediatr Rep"},{"issue":"4","key":"pone.0293949.ref031","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/j.anaerobe.2010.06.002","article-title":"Investigation of the intestinal microbiota in preterm infants using different methods","volume":"16","author":"C Roug\u00e9","year":"2010","journal-title":"Anaerobe"},{"issue":"3","key":"pone.0293949.ref032","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1203\/01.PDR.0000078274.74607.7A","article-title":"Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants","volume":"54","author":"A Schwiertz","year":"2003","journal-title":"Pediatr Res"},{"issue":"6","key":"pone.0293949.ref033","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.earlhumdev.2011.02.007","article-title":"Risk factors associated with gut and nasopharyngeal colonization by common Gram-negative species and yeasts in neonatal intensive care units patients","volume":"87","author":"\u00dc Parm","year":"2011","journal-title":"Early Hum Dev"},{"issue":"51","key":"pone.0293949.ref034","doi-asserted-by":"crossref","first-page":"E11988","DOI":"10.1073\/pnas.1810840115","article-title":"Estimating the proportion of bystander selection for antibiotic resistance among potentially pathogenic bacterial flora","volume":"115","author":"C Tedijanto","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"Number 01","key":"pone.0293949.ref035","doi-asserted-by":"crossref","first-page":"035","DOI":"10.1055\/s-2000-7290","article-title":"SEPTICEMIA DUE TO MULTIRESISTANT KLEBSIELLA PNEUMONIAE IN A NEONATAL UNIT: A CASE-CONTROL STUDY","volume":"17","author":"E Roilides","year":"2000","journal-title":"Am J Perinatol"},{"issue":"4","key":"pone.0293949.ref036","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1097\/00005176-200404000-00005","article-title":"Bacterial Colonization of the Neonatal Gut","volume":"38","author":"M. Pietzak","year":"2004","journal-title":"J Pediatr Gastroenterol Nutr"},{"issue":"3","key":"pone.0293949.ref037","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1038\/pr.2016.86","article-title":"Nasogastric feeding tubes from a neonatal department yield high concentrations of potentially pathogenic bacteria\u2014even 1 d after insertion","volume":"80","author":"SM Petersen","year":"2016","journal-title":"Pediatr Res"},{"issue":"1","key":"pone.0293949.ref038","doi-asserted-by":"crossref","first-page":"15948","DOI":"10.1038\/s41598-017-15769-9","article-title":"Rapid in situ imaging and whole genome sequencing of biofilm in neonatal feeding tubes: A clinical proof of concept","volume":"7","author":"P Ogrodzki","year":"2017","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0293949.ref039","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.jhin.2005.01.025","article-title":"A case-control study of risk factors associated with rectal colonization of extended-spectrum beta-lactamase producing sp. in newborn infants","volume":"61","author":"N Boo","year":"2005","journal-title":"J Hosp Infect"},{"issue":"4","key":"pone.0293949.ref040","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1016\/j.jhin.2007.01.014","article-title":"Healthcare-associated infections in neonatal units: lessons from contrasting worlds","volume":"65","author":"S Srivastava","year":"2007","journal-title":"J Hosp Infect"},{"issue":"1","key":"pone.0293949.ref041","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s40168-015-0126-1","article-title":"The first microbial environment of infants born by C-section: the operating room microbes","volume":"3","author":"H Shin","year":"2015","journal-title":"Microbiome"},{"issue":"1","key":"pone.0293949.ref042","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/2049-2618-2-1","article-title":"Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants","volume":"2","author":"B Brooks","year":"2014","journal-title":"Microbiome"},{"issue":"11","key":"pone.0293949.ref043","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1097\/00006454-200211000-00010","article-title":"Risk of resistant infections with Enterobacteriaceae in hospitalized neonates","volume":"21","author":"N Singh","year":"2002","journal-title":"Pediatr Infect Dis J"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0293949","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T18:24:09Z","timestamp":1699381449000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0293949"}},"subtitle":[],"editor":[{"given":"Monica","family":"Cartelle Gestal","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,11,7]]},"references-count":44,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,11,7]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0293949","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,7]]}}}